Differential expression of VEGF isoforms and VEGF164-specific receptor neuropilin-1 in the mouse uterus suggests a role for VEGF164 in vascular permeability and angiogenesis during implantation

Genesis

Volumn 26, Issue 3, 2000, Pages 213-224

  Halder, J B ^a   Zhao, X ^a   Soker, S ^b   Paria, B C ^a,c   Klagsbrun, M ^b   Das, S K ^a   Dey, S K ^a  

^a UNIVERSITY OF KANSAS MEDICAL CENTER   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

^c UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

Author keywords

Implantation; Mouse; Neuropilin 1; Uterus; VEGF; VEGFR2

Indexed keywords

NEUROPILIN; VASCULOTROPIN; VASCULOTROPIN RECEPTOR;

ANGIOGENESIS; ANIMAL EXPERIMENT; ARTICLE; BLOOD VESSEL PERMEABILITY; DECIDUALIZATION; EMBRYO DEVELOPMENT; MOUSE; NIDATION; NONHUMAN; PREGNANCY; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; BASE SEQUENCE; CAPILLARY PERMEABILITY; DNA PRIMERS; EMBRYO IMPLANTATION; ENDOTHELIAL GROWTH FACTORS; FEMALE; IN SITU HYBRIDIZATION; LYMPHOKINES; MICE; NEOVASCULARIZATION, PHYSIOLOGIC; NERVE TISSUE PROTEINS; NEUROPILIN-1; PROTEIN ISOFORMS; RNA, MESSENGER; UTERUS; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTORS;

ANIMALIA; MAMMALIA;

EID: 0034083613     PISSN: 1526954X     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1526-968X(200003)26:3<213::AID-GENE7>3.0.CO;2-M     Document Type: Article

References (68)

1. Brier G, Albrecht U, Sterrer S, Risau W. 1992. Expression of vascular endothelial growth factor during embryonic angiogenesis and endothelial cell differentiation. Development 114:521-532.
2. Carmeliet P, Ferreira V, Breier G, Pollefeyt S, Kieckens L, Harpal K, Eberhardt C. 1996. Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 380:435-439.
3. 188. Nature Med 5:495-502.
4. Chakraborty I, Das SK, Dey SK. 1995. Differential expression of vascular endothelial growth factor and its receptor mRNAs in the mouse uterus around the time of implantation. J Endocrinol 147:339-352.
5. Charnock-Jones DS, Sharkey AM, Rajput-Williams J, Burch D, Schofield JP, Fountain SA, Boocock CA, Smith SK. 1993. Identification and localization of alternately spliced mRNAs for vascular endothelial growth factor in human uterus and estrogen regulation in endometrial carcinoma cell lines. Biol Reprod 48:1120-1128.
6. Claffey KP, Wilkinson WO, Spiegelman BM. 1992. Vascular endothelial growth factor: Regulation by cell differentiation and activated second messenger pathways. J Biol Chem 267:16317-16322.
7. Cohen T, Gitay GH, Neufeld G, Levi BZ. 1992. High levels of biologically active vascular endothelial growth factor (VEGF) are produced by the baculovirus expression system. Growth Factors 7:131-138.
8. Conn G, Bayne ML, Soderman D, Kwok PW, Sullivan KA, Palisi TM, Hope DA, Thomas KA. 1990a. Amino acid and cDNA sequence of a vascular endothelial cell mitogen - that is homologous to platelet derived growth factor. Proc Natl Acad Sci USA 87:2628-2632.
9. Conn G, Sodderman DD, Schaeffer MT, Wile M, Hatcher VB, Thomas KA. 1990b. Purification of a glycoprotein: Vascular endothelial cell mitogen from a rat glioma derived cell line. Proc Natl Acad Sci USA 87:1323-1327.
10. Connolly DT, Olander JV, Heuvelman D, Nelson R, Monsell R, Haymore BL, Leimgruber R, Feder J. 1989. Human vascular permeability factor isolation from U937 cells. J. Biol Chem 264:20017-20024.
11. Cullinan-Bove K, Koos RD. 1993. Vascular endothelial growth factor/ vascular permeability factor expression in the rat uterus: Rapid stimulation by estrogen correlates with estrogen induced increases in uterine capillary permeability and growth. Endocrinology 133:829-837.
12. 3 in the mouse uterus: Analysis of the periimplantation period and effects of ovarian steroids. Endocrinology 130:3459-3466.
13. Das SK, Wang X-N, Paria BC, Damm D, Abraham JA, Klagsbrun M, Andrews GK, Dey SK. 1994. Heparin-binding EGF-like growth factor gene is induced in the mouse uterus temporally by the blastocyst solely at the site of its apposition: A possible ligand for interaction with blastocyst EGF-receptor in implantation. Development 120:1071-1083.
14. Das SK, Paria BC, Chakraborty I, Dey SK. 1995. Cannabinoid ligand-receptor signaling in the mouse uterus. Proc Natl Acad Sci USA 92:4332-4336.
15. Dey SK. 1996. Implantation. In: Adashi EY, Rock JA, Rosenwaks Z, editors. Reproductive endocrinology, surgery, and technology. Philadelphia: Lippincott-Raven. p 421-434.
16. Dvorak HF, Nagy JA, Feng D, Brown LF, Dvorak AM. 1999. Vascular permeability factor/vascular endothelial growth factor and the significance of microvascular hyperpermeability in angiogenesis. Curr Top Microbiol Immunol 237:97-132.
17. Enders AC, Schlafke S. 1967. A morphological analysis of the early implantation stages in the rat. Am J Anat 120:185-226.
18. Ferrara N, Davis-Smith T. 1997. The biology of vascular endothelial growth factor. Endocrine Rev 18:4-25.
19. Ferrara N, Henzel WJ. 1989. Pituitary follicular cells secrete a novel heparin-binding growth factor specific for vascular endothelial cells. Biochem Biophys Res Commun 116:851-858.
20. Ferrara N, Carver-Moore K, Chen H, Dowd M, Lu L, Orquote-Shea KS, Powell-Braxton L, Hillan KJ, Moore MW. 1996. Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature 380:439-442.
21. Folkman J, Klagsbrun M. 1987. Angiogenic factors. Science 235:442-447.
22. Fong GH, Rossant J, Gertsenstein M, Breitman ML. 1995. Role of the Flt-1 receptor tyrosine kinase in regulating the assembly of vascular endothelium. Nature 376:66-70.
23. Goodger AM, Rogers PA. 1993. Uterine endothelial cell proliferation before and after embryo implantation. J Reprod Fertil 99:451-457.
24. Han JA, Stratowa C, Rutter WJ. 1987. Isolation of full-length putative rat lysophospholipase cDNA using improved methods for mRNA isolation and cDNA cloning. Biochemistry 26:1617-1625.
25. He Z, Tessier-Lavigne M. 1997. Neuropilin is a receptor for the axonal chemorepellant semaphorin III. Cell 90:739-751.
26. Houck KA, Leung DW, Rowland AM, Winer J, Ferrara N. 1992. Dual regulation of vascular endothelial growth factor bioavailability by genetic and proteolytic mechanisms. J Biol Chem 267:26031-26037.
27. Huet YM, Andrews GK, Dey SK. 1989. Cell type-specific localization of c-myc protein in the mouse uterus: Modulation by steroid hormones and analysis of the periimplantation period. Endocrinology 125:1683-1690.
28. Hyder SM, Stancel GM. 1999. Regulation of angiogenic growth factors in the female reproductive tract by estrogen and progesterone. Mol Endocrinol 13:806-811.
29. Jakeman LB, Armanini M, Philips HS, Ferrara N. 1993. Developmental expression of binding sites and messengers ribonucleic acid for vascular endothelial growth factor suggests a role for this protein in vasculogenesis and angiogenesis. Endocrinology 133:848-859.
30. Joukov V, Pajusola K, kaipainen A, Chilov D, Lahtinen I, Kukk E, Saksela O, Kalkkinen N, Alitalo K. 1996. A novel vascular endothelial growth factor, VEGF-C, is a ligand for the Flt4 (VEGFR-3) and KDR (VEGFR-2) receptor tyrosine kinases. EMBO J 15:290-298.
31. Kalodkin AL, Levengood DV, Rowe EG, Tai YT, Giger RJ, Ginty DD. 1997. Neuropilin is semaphorin III receptor. Cell 90:753-762.
32. Kawakami A, Kitsukawa T, Takagi S, Fujisawa H. 1995. Developmentally regulated expression of a cell surface protein, Neuropilin in the mouse nervous system. J Neurobiol 29:1-17.
33. Kitsukawa T, Shimono A, Kawakami A, Kondoh H, Fujisawa H. 1995. Overexpression of a membrane protein, neuropilin, in chimeric mice causes anomalies in the cardiovascular system, nervous system and limbs. Development 121:4309-4318.
34. Kitsukawa T, Shimizu M, Sanbo M, Hirata T, Taniguchi M, Bekku Y, Fujisawa H. 1997. Neuropilin-semaphorin III/D-mediated chemorepulsive signals play a crucial role in peripheral nerve projection in mice. Neuron 19:995-1005.
35. Lim H, Gupta RA, Ma W-G, Paria BC, Moller DE, Morrow JD, DuBois RN, Trzaskos JM, Dey SK. 1999. Cyclo-oxygenase-2-derived prostacyclin mediates embryo implantation in the mouse via PPARδ. Genes Dev 13:1561-1574.
36. Lobb RR, Key ME, Alderman EM, Fett JW. 1985. Partial purification and characterization of a vascular permeability factor secreted by a human colon adenocarcinoma cell line. Int J Cancer 36:473-478.
37. Maglione D, Guerriero V, Viglietto G, Delli-Bovi P, Persico MG. 1991. Isolation of a human placenta cDNA coding for a protein related to the vascular permeability factor. Proc Natl Acad Sci USA 88:9267-9271.
38. Matthews W, Jordan CT, Gavin M, Jenkins NA, Copeland NG, Lemischchka IR. 1991. A receptor tyrosine kinase cDNA isolated from a population of enriched primitive hemopoietic cells and exhibiting close genetic linkage to c-kit. Proc Natl Acad Sci USA 88:9026-9030.
39. Millauer B, Wizigmann VS, Schnurch H, Martinez R, Moller NPH, Risau W, Ullrich A. 1993. High affinity VEGF binding and developmental expression suggest Flk-1 as a major regulator of vasculogenesis and angiogenesis. Cell 72:835-846.
40. Muller YA, Christinger HW, Keyt BA, de Vos AM. 1997. The crystal structure of vascular endothelial growth factor (VEGF) refined to 1.93 A resolution: Multiple copy flexibility and receptor binding. Structure 5:1325-1338.
41. Neufeld G, Tessler S, Gitay-Goren H, Cohen T, Levi BZ. 1999. Vascular endothelial growth factor and its receptors. Prog Growth Factor Res 5:89-97.
42. Paria BC, Jones KL, Flanders KC, Dey SK. 1992. Localization and binding of transforming growth factor-β isoforms in mouse preimplantation embryos and in delayed and activated blastocysts. Dev Biol 151:91-104.
43. Paria BC, Huet-Hudson YM, Dey SK. 1993. Blastocyst's state of activity determining the window of implantation in the respective mouse uterus. Proc Natl Acad Sci USA 90:10159-10162.
44. Paria BC, Zhao X, Das SK, Dey SK, Yoshinaga K. 1999. Zonula Occludens-1 and E-cadherin are coordinately expressed in the mouse uterus with the initiation of implantation and decidualization. Dev Biol 208:488-501.
45. Parr EL, Tung HN, Parr MB. 1987. Apoptosis as the mode of uterine epithelial cell death during embryo implantation in mice and rats. Biol Reprod 36:211-225.
46. Peters KG, Devries C, Williams LT. 1993. Vascular endothelial growth factor expression during embryogenesis and tissue repair suggests a role in endothelial differentiation and blood vessel growth. Proc Natl Acad Sci USA 90:8915-8919.
47. PlouetJ, Schilling J, Gospodarowicz D. 1989. Isolation and characterization of a newly identified endothelial cell mitogen produced by AtT-20 cells. EMBO J 8:3801-3806.
48. Psychoyos A. 1973. Endocrine control of egg implantation. In: Greep RO, Astwood EG, Geiger SR, editors. Handbook of physiology. Washington DC: American Physiological Society, p 187-215.
49. Quinn TP, Peters KG, De Vris D, Ferrara N, Williams LT. 1993. Fetal liver kinase 1 is a receptor for vascular endothelial growth factor and is selectively expressed in vascular endothelium. Proc Natl Acad Sci USA 90:7533-7537.
50. Risau W. 1997. Mechanisms of angiogenesis. Nature 386:671-674.
51. Sambrook J, Fritsch EF, Maniatis T. 1989. Molecular cloning: A laboratory manual. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press.
52. Schlafke S, Enders A. 1975. Cellular basis of interaction between trophoblast and uterus at implantation. Biol Reprod 12:41-65.
53. 2 terminal amino acid sequence of guinea pig tumor secreted vascular permeability factor. Cancer Res 50:1774-1778.
54. Shalaby F, Rossant J, Yamaguchi TP, Gertsenstein M, Wu XF, Breitman ML, Schuh AC. 1995. Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature 376: 62-66.
55. Shibuya M, Yamaguchi S, Yamane A, Ikeda T, Tojo A, Matsushime H, Sato M. 1990. Nucleotide sequence and expression of a novel human receptor type tyrosine kinase (fit) closely related to the fms family. Oncogene 5:519-524.
56. Shima DT, Kuroki M, Deutsch U, Ng Y-S, Adamis AP, Drquote APA. 1996. The mouse gene for vascular endothelial growth factor. Genomic structure, definition of the transcriptional unit and characterization of transcriptional and post-transcriptional regulatory sequences. J Biol Chem 271:3877-3883.
57. Shweiki D, Ltin A, Neufeld G, Gitay-Goren H, Keshet E. 1993. Patterns of expression of vascular endothelial growth factor (VEGF) and VEGF receptors in mice suggest a role in hormonally regulated angiogenesis. J Clin Invest 19:2235-2243.
58. 165 via its exon 7-encoded domain. J Biol Chem 271:5761-5767.
59. 165. J Biol Chem 272: 31582-31588.
60. Soker S, Takashima S, Miao HQ, Neufeld G, Klagsbrun M. 1998. Neuropilin-1 is expressed by endothelial and tumor cells as an isoform specific receptor for vascular endothelial growth factor. Cell 92: 735-745.
61. Sugihara T, Wadhwa R, Kaul SC, Mitsui Y. 1998. A novel alternatively spliced form of murine vascular endothelial growth factor VEGF-115. J Biol Chem 273:3033-3038.
62. Takagi S, Kasuya Y, Shimizu M, Matsuura T, Tsuboi M, Kawakami A, Fujisawa H. 1995. Expression of a cell adhesion molecule, neuropilin in the developing chick nervous system. Dev Biol 170:207-222.
63. Tischer E, Mitchell R, Hartmann T, Silva M, Gospodarowicz D, Fiddes JC, Abraham J. 1991. The human gene for vascular endothelial growth factor. J Biol Chem 266:11947-11954.
64. Waltenberger J, Claesson WL, Siegbahn A, Shibuya M, Heldin CH. 1994. Different signal transduction properties of KDR and Flt1, two receptors for vascular endothelial growth factor. J Biol Chem 269:26988-26995.
65. Welsh AO. 1993. Uterine cell death during implantation and early placentation. Microscope Res Tech 25:223-245.
66. Welsh AO, Enders AC. 1987. Trophoblast-decidual cell interactions and establishment of maternal blood circulation in the parietal yolk sac placenta of the rat. Anat Rec 217:203-219.
67. Welsh AO, Enders AC. 1991. Chorioallantoic placenta formation in the rat: II. Angiogenesis and maternal blood circulation in the mesometrial region of the implantation chamber prior to placenta formation. Am J Anat 192:347-365.
68. Yoshida A, Anand-Apte B, Zetter BR. 1996. Differential endothelial migration and proliferation to basic fibroblast growth factor and vascular endothelial growth factor. Growth Factors 13:57-64.